University of Groningen
Interview-based cross-sectional needs assessment to advance the implementation of an
effective antibiotic stewardship program in Indonesian hospitals
Woerdenbag, Herman; Hak, Eelko
Published in:
Health Policy OPEN
DOI:
10.1016/j.hpopen.2019.100002
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from
it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date:
2020
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Woerdenbag, H., & Hak, E. (2020). Interview-based cross-sectional needs assessment to advance the
implementation of an effective antibiotic stewardship program in Indonesian hospitals. Health Policy OPEN,
1, [100002]. https://doi.org/10.1016/j.hpopen.2019.100002
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum.
Interview-based cross-sectional needs assessment to advance the
implementation of an effective antibiotic stewardship program in
Indonesian hospitals
Fauna Herawati
a,b,⁎
, Sheny Clarin Ananta
a, Ida Ayu Andri Parwitha
a, Sylvan Septian Ressandy
a,
Nur Laili Rahmatin
a, Nur A
fifah Rachmadini
a, Veronika Ayu Tangalobo
a, Setiasih
c, Rika Yulia
a, Eelko Hak
d,
Herman J. Woerdenbag
e, Christina Avanti
faDepartment of Clinical and Community Pharmacy, Faculty of Pharmacy, Universitas Surabaya, Jalan Raya Kalirungkut, Surabaya 60293, Indonesia bDepartment of Pharmacology and Clinical Pharmacy, Faculty of Pharmacy, Universitas Indonesia, Depok 16424, Indonesia
cDepartment of Developmental Psychology, Faculty of Psychology, Universitas Surabaya, Jalan Raya Kalirungkut, Surabaya 60293, Indonesia dDepartment of PharmacoTherapy, -Epidemiology& -Economy, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, the Netherlands eDepartment of Pharmaceutical Technology and Biopharmacy, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, the Netherlands fDepartment of Pharmaceutics, Faculty of Pharmacy, Universitas Surabaya, Jalan Raya Kalirungkut, Surabaya 60293, Indonesia
A B S T R A C T A R T I C L E I N F O
Article history: Received 24 July 2019 Accepted 1 December 2019 Available online 07 January 2020
Antibiotic resistance has become a global health issue, negatively affecting the quality and safety of patient care, and increasing medical expenses, notably in Indonesia. Antibiotic stewardship programs (ASPs) aim to reduce resistance rates and their implementation in hospitals, has a high priority worldwide.
We aimed to monitor the progress in the organizational implementation of ASPs in Indonesian hospitals by an Antimi-crobial Resistance Control Program (ARCP) team and to identify possible hurdles. We conducted a cross-sectional study with structured interviews based on a checklist designed to assess the achievement of structural indicators at the organizational level in four private and three public hospitals in four regions (Surabaya, Sidoarjo, Mojokerto, Bangil) in East Java, Indonesia.
The organizational structure of public hospitals scored better than that of private hospitals. Only three of the seven hos-pitals had an ARCP team. The most important deficiency of support appeared to be insufficient funding allocation for information technology development and lacking availability and/or adherence to antibiotic use guidelines. The stud-ied hospitals are, in principle, prepared to adequately implement ASPs, but with various degrees of eagerness. The hos-pital managements have to construct a strategic plan and to set clear priorities to overcome the shortcomings.
© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Keywords: Antibiotic stewardship Structural indicators Needs assessment Hospital Indonesia Key messages
There is an obvious need for sufficient resources for information tech-nology development, for dissemination of guidelines for antibiotic use, and for provision of information about the use of appropriate antibiotics to educate patients.
1. Introduction
Any use of antibiotics will contribute to antibiotic resistance, including the appropriate use of antibiotics. Antibiotic resistance is caused by the mu-tation of pathogenic micro-organisms, following inappropriate and super-fluous use of antibiotics [1,2]. An antibiotic resistance study by the Indonesia Agency for Health Research and Development, Indonesian Minis-try of Health (Badan Litbang Kesehatan Indonesia 2013) reported during a seminar in 2014, revealed that in six public hospitals in Indonesia the prev-alence of extended-spectrumβ-lactamase in isolates of E. coli was 45%, in isolates of K. pneumonia 42%, and in isolates of K. oxytoca 26% [3].
Antibiotic resistance is a serious worldwide health problem that jeopar-dizes the quality and safety of patient care and may substantially increase treatment costs. For these reasons the World Health Organization (WHO)
Health Policy OPEN 1 (2020) 100002
⁎ Corresponding author at: Faculty of Pharmacy, Universitas Surabaya, Jalan Raya Kalirungkut, FF Building, 5th Floor, Surabaya 60293, Indonesia.
E-mail addresses:fauna@staff.ubaya.ac.id, (F. Herawati),setiasih@staff.ubaya.ac.id, (Setiasih), rika_y@staff.ubaya.ac.id, (R. Yulia),e.hak@rug.nl, (E. Hak),h.j.woerdenbag@rug.nl, (H.J. Woerdenbag),c_avanti@staff.ubaya.ac.id. (C. Avanti).
http://dx.doi.org/10.1016/j.hpopen.2019.100002
2590-2296/© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4. 0/).
Contents lists available atScienceDirect
Health Policy OPEN
and the Center for Disease Control and Prevention (CDC) emphasize the ne-cessity for every hospital worldwide to implement an antibiotic steward-ship program in order to prevent the development of antibiotic resistance
[1,3]. The implementation of antibiotic stewardship programs in
Indonesia is achieved by the establishment of an Antimicrobial Resistance Control Program (ARCP) team in all hospitals as stipulated in the Ministry of Health Regulation of the Republic of Indonesia No. 8 Year 2015 [4]. The ARCP is a new important standard for hospital accreditation in this country (Standar Nasional Akreditasi Rumah Sakit, SNARS) published in 2017 [5,6]. Therefore, in 2018 an assessment of the ARCPs was conducted by a hospital accreditation committee in every hospital in Indonesia for the purpose of hospital accreditation [5]. The ongoing high rates of antibiotic resistance in Indonesia, however indicate that the implementation of ARPs in most hospitals has not adequately been achieved, possibly due to a lack of facilities, infrastructure and strategies such as audits and feedback [7].
Strategies and priorities to provide resources to overcome the problems with implementation of antibiotic stewardship are based on a hospital's in-dividual policy. Several studies reported that the needed resources required not only include audits and feedback by antibiotic stewardship teams but also comprise the purchase of information technology and software as well as the set-up of a microbiology laboratory [8]. There is a study in a sin-gle large tertiary care teaching medical center, where a stewardship pro-gram was considered part of the infection control propro-gram and no additional resources were required [9].
1.1. The aim of the study
To make a complete ARCP needs assessment, we aimed to assess the ful-fillment of four domains (organization structure, leader support, internal and external factors, and information availability) necessary for the organi-zational implementation of antibiotic stewardship programs in selected pri-vate and public hospitals in Indonesia.
2. Materials and methods
We conducted a cross-sectional study with structured interviews in
which observations were made using a questionnaire (Appendix 1)
de-signed to assess the achievement of structural indicators at the
organiza-tional level of hospitals. InTable 1demographic details of the seven
hospitals included in this study are listed. The hospitals were selected based on their nature (public versus private), variety in number of beds, dif-ferent levels of care provided and location (East Java, Indonesia).
Hospital classification in Indonesia is done according to the Ministry of Health regulations [10]. There are three levels of care in the Indonesian health system. The primary care is a health facility providing a patient's first access to the health care. If specialized care is needed, the patient can be referred promptly to secondary (a secondary hospital) or tertiary
care (a tertiary hospital) [11,12]. The Indonesian health system has a mix-ture of public and private providers andfinancing [13,14].
The questionnaire was based on CDC Core Elements of Hospital Antibi-otic Stewardship Programs [15], Structural Indicators for Evaluating Anti-microbial Stewardship Programs in European Hospitals [16], the Belgian Antibiotic Policy Coordination Committee (BAPCOC) (used in Belgium, Europe and America for auditing the quality of antibiotic stewardship
pro-grams) [17], and National Standards for Hospital Accreditation in
Indonesia [5,6]. The respondent (one for each hospital) was the person in charge of the hospital management who was responsible for the medical service to the patients. The interviews were performed by the authors. To ensure validity of interview result per respondent, the interview results were compared to document observation results by the authors, including circular letters of director, operational standards manuals, antibiotic usage manuals, formularies, hospital antibiogram, and antibiotic resistance prevalence reports available in the hospital. We attributed score 2 (Table 2, Internal and External Factors of the Hospital) in case a document was avail-able support the interview. The results were presented to and discussed with the hospital staff. What we found was fully acknowledged and already recognized by them.
In the questionnaire four domains were distinguished: organizational structure, leader support, internal and external factors of the hospital, and information availability (Appendix 1), each with a number of questions (items), that were answered by the interviewed staff. These domains were based on the sources [5,6,15–17] used to compile the questionnaire. In the analysis, the scores per item within a domain and overall were summed (Table 2). The total score per hospital was divided by the maximum score of 40 points and multiplied by 10. We subdivided a scale of 0–3 as “low” ARCP implementation; scale 4–6 as “intermediate” ARCP implementation; scale 7–10 as “high” ARCP implementation.
3. Results
Not all hospitals under study had an ARCP team. Only one hospital allo-cated funds for information technology (IT) development. All hospitals had a policy for the medical doctors with respect to antibiotic use. Nearly all hospitals had an antibiogram. The antibiotic stewardship implementation scores between hospitals varied, from low (hospitals A and B), to interme-diate (hospitals C, D, and E), and high (hospitals F and G) (seeTable 2).
Of the three public (governmentfinanced) hospitals, two had an ARCP
team installed. Two hospitals were in the readiness stage from an organiza-tional perspective (score 9 out of 10), three hospitals were in the intermedi-ate readiness stage (4.5/10, 4.5/10, 5.5/10 respectively), and two hospitals was in the early readiness stage (1/10, 2/10) of implementing the antibiotic stewardship program (seeTable 2). The data from the seven participating private and public hospitals show that the stage of developing ARCP varied. One hospital (hospital A) was not ready to implement the antibiotic stew-ardship program; it merely had a policy for the doctors to prescribed antibi-otic and the antibiogram.
Table 1 Hospital demography. Characteristics A B C D E F G Hospital classificationa B B B C A B C
Levels of care A tertiary hospital A tertiary hospital A tertiary hospital A secondary hospital
A tertiary hospital A tertiary hospital A secondary hospital
Number of bed 117 172 235 225 467 134 109
Area geographical Surabaya municipality
Mojokerto regency Surabaya municipality
Sidoarjo regency Sidoarjo regency Surabaya municipality
Bangil district
Ownership Private Government (public)
Private Private Government (public)
Private Government (public)
a According to Ministry of Health Republic of Indonesia (MoH-RI). [Peraturan Menteri Kesehatan No. 56 tahun 2014: Klasifikasi dan perizinan rumah sakit]: MoH-RI;
2014.
F. Herawati et al. Health Policy OPEN 1 (2020) 100002
Among the four domains, from lowest score to the highest score, leader support and information availability had the lowest average score (6.8), the subsequent domains were organization structure (7.2), internal and exter-nal factors (7.6).
Descriptive analysis of all potential barriers revealed that in all partici-pating hospitals fund allocation for IT development and availability of guidelines for antibiotic use were not well developed or even absent.
Organizational aspects that were well developed in all hospitals in-cluded the presence of a hospital pharmacist as part of the ARCP team, the provision of educational information from the management, the avail-ability of information for doctors on the appropriate type and dosing and administration of antibiotics, and the distribution of antibiogram through-out the wards.
4. Discussion
Similar to other developing countries, addressing antibiotic resistance in Indonesia requires a systems perspective. For the successful implementa-tion of a sustainable and comprehensive antibiotic stewardship program in
hospitals, leadership, commitment, and sufficient funding are needed
[18–21]. The results of the Organization Structure domain show that less than 50% of the hospitals have an ARCP team. ARCP serves to control the use of antibiotics to reduce the incidence of antibiotic resistance.
The relevance of an ARCP is supported by a systematic review of 32 studies by Baur et al. showing that the implementation of antibiotic stew-ardship programs for at home illness in 19 countries could significantly
re-duce 51% of incidence of infection, 48% of extended-spectrum
β-lactamase-producing Gram-negative bacteria, 37% of methicillin-resistant Staphylococcus aureus, and 32% the incidence of Clostridium difficile
infec-tions [22]. Based on this research evidence it was recommended that
every hospital should immediately start the implementation of formation of an ARCP. Not only the availability of ARCP team but also multidisciplin-ary communication among professionals is a critical point to the success of the ASP implementation [23].
From the scores of the Leader Support domain, it appears that less than 50% of the hospitals had fund allocation for ARCP and that only 14% of the hospitals had fund allocation for IT development. In 1999 The Belgian An-tibiotic Policy Coordination Committee (BAPCOC) created a situation in which all acute care hospitals in the country receivedfinancial and techni-cal support for hiring a trained manager for their antimicrobial manage-ment teams. This intervention, the antimicrobial managemanage-ment teams and the antimicrobial management teams funding, improved the antimicrobial use for patients admitted to hospital for pneumonia and lower limb surgery between 1999 and 2010 in Belgium [24]. Based on this information, fund allocation is strongly recommended for needed supports for the ARCP in each hospital.
The study by Van Limburg et al. aimed at analyzing progress and obsta-cles in the implementation of the antibiotic stewardship program at nine hospitals in the Netherlands (three educational and six non-educational hospitals) [25]. It was shown that only 25% of educational hospitals and 18% non-educational hospitals had implemented IT for antibiotic steward-ship programs. According to the CDC, the role of IT in the integration of an-tibiotic stewardship with the services provided at a hospital is imperative. This role includes giving support for decisions regarding antibiotic prescrip-tions, providing facilities for the collection and reporting of antibiotic use, as well as providing information and protocols that can be directly linked to ARCP or clinical pathways owned by the hospital, thereby potentially im-proving the rational use of medicines [9]. Thisfinding is supported by the study by Charani et al. showing that there was an insignificant increase in the adherence to the use of antibiotics on empirical therapy in the treat-ment of hospitalized patients [26]. The increase was significant, however,
in the operating theater. In addition, there was an increased (but insignifi-cant) percentage in documenting a stop/review date regarding the prescrip-tion of hospitalized patients. Based on this research evidence, it is necessary to allocate funds for IT development in order to realize the optimum goals of an effective ARCP at each hospital.
Research on the internal and external factors of the hospital showed that the availability of guidelines for antibiotic use was in the low category,
Table 2
The hospitals readiness in the implementation of antibiotic stewardship.
No. Components Max score A B C D E F G Total (%)
1.
Organizational structure
Availability of ARCP team 2 0 0 0 0 2 2 2 6 (43)
Multidisciplinary communication 2 0 2 0 2 2 0 2 8 (57)
Multidisciplinary in ARCP 2 0 0 0 0 2 2 2 6 (43)
Doctor as ARCP leader 2 0 0 0 0 2 2 2 6 (43)
Presence of clinical pharmacist 2 0 2 0 2 2 2 2 10 (71)
Total 10 0 4 0 4 10 8 10
2.
Leader support
Formal statement of ARCP team establishment 2 0 0 2 0 2 2 2 8 (57)
Fund allocation for ARCP 2 0 0 2 0 0 2 2 6 (43)
Fund allocation for health personnel education 2 0 0 2 0 2 2 2 8 (57)
Fund allocation for IT development 2 0 0 2 0 0 0 0 2 (14)
Provision of education 2 0 0 2 2 2 2 2 10 (71)
Total 10 0 0 10 2 6 8 8
3.
Internal and external factors of the hospital
Availability of policy for the doctor to administer doses, amounts, and direction of antibiotic use in hospital 2 2 2 2 2 2 2 2 14 (100) Availability of antibiotic use guidelines (Pedoman Penggunaan Antibiotik, PPAB) 2 0 0 0 0 0 2 2 4 (29) Availability of operational standards for audit and feedback by pharmacy 2 0 0 0 2 0 2 2 6 (43)
Policy of antibiotic use 2 0 0 0 2 2 2 0 6 (43)
Access of guidelines/journal 2 0 0 2 2 0 2 2 8 (57)
Total 10 2 2 4 8 4 10 8
4.
Information availability
Availability of data on the level of antibiotic use (DDD/100 bed-days) 2 0 2 0 0 0 2 2 6 (43) Socialization of the prevalence of resistant bacteria to prescriber 2 0 0 2 0 0 2 2 6 (43) Distribution of antibiograms throughout the wards 2 2 0 2 2 0 2 2 10 (71) Distribution of formularies to the entire wards 2 0 0 0 0 2 2 2 6 (43) Information on the wise use of antibiotics for patients 2 0 0 0 2 0 2 2 6 (43)
Total 10 2 2 4 4 2 10 10
Total 4 8 18 18 22 36 36
because not all hospitals have guidelines for antibiotic use. The study by Van Limburg et al. showed that 88% of educational hospitals and 73% of non-educational hospitals implement antibiotic formulary for antibiotic stewardship program [25]. Guidelines for Antibiotic Use is a guideline ac-cording to the types of infections in patients or as prophylaxis for surgery [27,28]; therefore an ARCP can assist in the selection of antibiotics. Accord-ing to the IDSA's guideline, the development of Guidelines for Antibiotic Use from recent literature and antibiotic resistance reports is an additional component for implementing antibiotic stewardship. This is supported by a study reporting that the use of Guidelines for Antibiotic Use in intensive care unit (ICU) could reduce approximately 77% of antibiotic use and treat-ment costs, decrease patient mortality resulting from infections and de-crease the length of stay in ICU compared to before using an ARCP as a guide for choosing antibiotic therapy [29]. Based on this information, it is recommended that each hospital immediately starts to prepare guidelines for antibiotic use to be used in the rational and responsible selection of an-tibiotic therapy.
The results of the research on the information availability domain showed that only 43% hospitals provide information to the patient to use antibiotics wisely. Hospitals provide information on the rational use of antibiotics through leaflets, posters and light-emitting diode (LED) banner displays for both outpatients and inpatients, as there are several out-of-hospital patients who still continue to consume antibiotics in accor-dance with the duration of administration. Research conducted by Eells et al. in 188 patients with skin infections aimed to determine the adherence to the use of antibiotics during out-of-hospital care [30]. This study showed that patients had poor adherence to antibiotic use after checking out of hos-pital with worsening clinical outcomes.
Based on Rosenstock's Health Belief Model (HBM) theory, there are several construct determinants for the likelihood behavior (i.e. individ-ual perception), some modifying factors (age, sex, ethnicity, personal-ity, socioeconomic, knowledge), and cues to action. Knowledge is a modifiable factor and the perception of the provision of information to
patients is useful for improving their knowledge [31]. Knowledge is
one of the factors that influence our beliefs, which in turn affects behav-ior such as an increase in the adherence to the use of antibiotics as a means to improve the success of therapy and prevent antibiotic
resis-tance. This is in line with a study conducted by Munoz et al. [32],
where 126 patients were divided into two groups: 62 patients in the in-tervention group and 64 patients in the control group. The results showed that there was a significant difference in the level of conformity between the intervention group that was educated and the control group. Based on this information, it is recommended that each hospital provides reliable information regarding the use of antibiotics to patients
through leaflets, posters and LED banner displays as an appropriate
form of action and a means to increase the rational use of antibiotic. 5. Conclusions
The studied hospitals are, in principle, ready to implement adequate ASPs, but with various degrees of readiness. The main barriers are a lack of fund allocation for IT development (6/7) and unavailability of guidelines for antibiotic use (5/7). Every hospital should immedi-ately start to implement an ARCP according to Indonesian national standards.
Abbreviations
ARCP Antimicrobial Resistance Control Program
ASPs Antibiotic stewardship programs
BAPCOC The Belgian Antibiotic Policy Coordination Committee
CDC The Center for Disease Control and Prevention
HBM Health Belief Model
ICU Intensive care unit
IT Information technology
LED Light-emitting diode
Menristekdikti Menteri Riset, Teknologi dan Pendidikan Tinggi (Ministry of Research, Technology and Higher Education of the Repub-lic of Indonesia)
SNARS Standar Nasional Akreditasi Rumah Sakit (National
Stan-dards for Hospital Accreditation)
WHO The World Health Organization
Acknowledgements
This study was conducted in the framework of a collaboration agree-ment between the Faculty of Pharmacy University of Surabaya, Jalan Raya Kalirungkut, Surabaya and the Groningen Research Institute of Pharmacy, Faculty of Science and Engineering, University of Groningen, The Netherlands. We would like to thank to Erik Christopher, Klinik Bahasa, Faculty Kedokteran, Universitas Gadjah Mada (Yogyakarta) for helping to edit the manuscript.
Declaration of competing interest
The authors declare that they have no conflict of interest. Author contributions
FA was conceptualization and made the original draft the manuscript. The interviews were performed and the interview results were compared to document observation results by the authors SC, IA, SS, NL, NA, VA. HJW was writing, reviewing and editing. S, RY, EH, CA were reviewing and editing.
Ethics approval and consent to participate
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The written consent to par-ticipate were obtain from study participant. The study was approved by the respective hospital managements and was conducted in accordance with the Indonesian Law for the Protection of Personal Data. The study was ethically cleared by the Health Research Ethics Committee of Politeknik Kesehatan Kemenkes Surabaya, Kementerian Kesehatan No. 025/S/KEPK/V/2017.
Consent for publication
Interview participants received a participant information sheet and gave written consent.
Availability of data and materials Not applicable.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
F. Herawati et al. Health Policy OPEN 1 (2020) 100002
F. Herawati et al. Health Policy OPEN 1 (2020) 100002
References
1. Centers for Disease Control and Prevention (CDC). Antibiotic resistance threats in the United States, 2013. Atlanta: CDC; 2013 Available from https://www.cdc.gov/ drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf, Accessed date: 18 April 2016.
2. Lin J, Nishino K, Roberts MC, Tolmasky M, Aminov RI, Zhang L. Mechanisms of antibiotic resistance. Front Microbiol 2015;6(34).https://doi.org/10.3389/fmicb.2015.00034. 3. Siswanto [Seminar Nasional]. Kajian Resistensi Antimikroba dan Situasinya pada
Manusia di Indonesia. Jakarta: Center for Indonesian Veterinary Analytical Studies (CIVAS) http://civas.net/cms/assets/uploads/2014/03/Kajian-Resistensi-Antimikrobial-dan-Situasinya-pada-Manusia-di-Indonesia.pdf; 2014, Accessed date: 18 April 2016. 4.Ministry of Health Republic of Indonesia (MoH-RI). Peraturan Menteri Kesehatan No.
8 tahun 2015: Program pengendalian resistensi antimikroba di rumah sakit. MoH-RI; 2014.
5.Ministry of Health Republic of Indonesia (MoH-RI). Peraturan Menteri Kesehatan Republik Indonesia No. 34 tahun 2017: Akreditasi rumah sakit. MoH-RI; 2017. 6.Indonesian Commission for Hospital Accreditation (ICHA). Standar Nasional Akreditasi
Rumah Sakit Edisi 1. Komisi Akreditasi Rumah Sakit (KARS); 2017.
7. Parathon H, Kuntaman K, Widiastoety TH, Muliawan BT, Karuniawati A, Qibtiyah M, Djanun Z, Tawilah JF, Aditama T, Thamlikitkul V, Vong S. Progress towards antimicro-bial resistance containment and control in Indonesia. BMJ 2017;358:j3808.https://doi. org/10.1136/bmj.j3808.
8. Wagner B, Filice GA, Drekonja D, Greer N, MacDonald R, Rutks I, Butler M, Wilt TJ. An-timicrobial stewardship programs in inpatient hospital settings: a systematic review. In-fect Control Hosp Epidemiol 2014;35(10):1209–28.https://doi.org/10.1086/678057 [Epub 2014 Aug 21].
9. Stenehjem E, Hyun DY, Septimus E, Yu KC, Meyer M, Raj D, Srinivasan A. Antibiotic stewardship in small hospitals: barriers and potential solutions. Clin Infect Dis 2017;65 (4):691–6.https://doi.org/10.1093/cid/cix407.
10.Ministry of Health Republic of Indonesia (MoH-RI). Peraturan Menteri Kesehatan No. 56 tahun 2014: Klasifikasi dan perizinan rumah sakit. MoH-RI; 2014.
11.Ministry of Health Republic of Indonesia (MoH-RI). Peraturan Menteri Kesehatan No. 71 tahun 2013: Pelayanan kesehatan pada jaminan kesehatan nasional. MoH-RI; 2013. 12.Hensher M, Price M, Adomakoh S. Referral hospitals. In: Jamison DT, Breman JG,
Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P, editors. Dis-ease control priorities in developing countries. 2nd ed. New York: Oxford University Press; 2006.
13. Heywood P, Harahap NP. Health facilities at the district level in Indonesia. Aust New Zealand Health Policy 2009;6:13.https://doi.org/10.1186/1743-8462-6-13.
14. Mahendradhata Y, Trisnantoro L, Listyadewi S, Soewondo P, Marthias T, Harimurti P, Prawira J. The Republic of Indonesia health system review. Health Syst Transit 2017;7(1):1–292. http://apps.who.int/iris/bitstream/handle/10665/254716/ 9789290225164-eng.pdf;jsessionid=C14704A620474D133474DEFDDD9E5003? sequence=1.
15. Centers for Disease Control and Prevention. Core elements of hospital antibiotic steward-ship programs. Atlanta, GA: US Department of Health and Human Services, CDC; 2014. http://www.cdc.gov/getsmart/healthcare/implementation/core-elements.html, Accessed date: 18 April 2016.
16. Buyle FM, Metz-Gercek S, Mechtler R, Kern WV, Robays H, Vogelaers D, Struelens MJ. Development and validation of potential structure indicators for evaluating antimicrobial stewardship programmes in European hospitals. Eur J Clin Microbiol Infect Dis 2013;32 (9):1161–70.https://doi.org/10.1007/s10096-013-1862-4[Epub 2013 Mar 23]. 17.Balligand E, Costers M, Van Gastel E. Belgian Antibiotic Policy Coordination Committee:
policy paper for the 2014– 2019 term. Belgian Antibiotic Policy Coordination Committee (BAPCOC); 2014.
18. Merrett GL, Bloom G, Wilkinson A, MacGregor H. Towards the just and sustainable use of antibiotics. J Pharm Policy Pract 2016;9:31. https://doi.org/10.1186/s40545-016-0083-5.
19.James RS, McIntosh KA, Luu SB, Cotta MO, Marshall C, Thursky KA, Buising KL. Antimi-crobial stewardship in Victorian hospitals: a statewide survey to identify current gaps. Med J Aust 2013;199(10):692–5.
20. Cairns KA, Roberts JA, Cotta MO, Cheng AC. Antimicrobial stewardship in Australian hospitals and other settings. Infect Dis Ther 2015;4(Suppl. 1):27–38.https://doi.org/ 10.1007/s40121-015-0083-9[Epub 2015 Sep 11].
21. Leung V, Wu JH, Langford BJ, Garber G. Landscape of antimicrobial stewardship pro-grams in Ontario: a survey of hospitals. CMAJ Open 2018;6(1):E71–6.https://doi.org/ 10.9778/cmajo.20170111.
22. Baur D, Gladstone BP, Burkert F, Carrara E, Foschi F, Döbele S, et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacte-ria and Clostridium difficile infection: a systematic review and meta-analysis. Lancet Infect Dis 2017;17(9):990–1001.https://doi.org/10.1016/S1473-3099(17)30325-0[Epub 2017 Jun 16].
23. Setiadi A, Wibowo Y, Herawati F, Irawati S, Setiawan E, Presley B, Zaidi MA, Sunderland B. Factors contributing to interprofessional collaboration in Indonesian health centres: a focus group study. J Interprofessional Educ Pract 2017;8:69–74.https://doi.org/10. 1016/j.xjep.2017.06.002.
24. Lambert ML, Bruyndonckx R, Goossens H, Hens N, Aerts M, Catry B, Neely F, Vogelaers D, Hammamiet N. The Belgian policy of funding antimicrobial stewardship in hospitals and trends of selected quality indicators for antimicrobial use, 1999–2010: a longitudinal study. BMJ Open 2015;5:e006916.https://doi.org/10.1136/bmjopen-2014-006916.
25. Van Limburg M, Sinha B, Lo-Ten-Foe JR, van Gemert-Pijnen JE. Evaluation of early implementations of antibiotic stewardship program initiatives in nine Dutch hospi-tals. Antimicrob Resist Infect Control 2014;3(33). https://doi.org/10.1186/2047-2994-3-33.
26. Charani E, Gharbi M, Moore LSP, Castro-Sanchéz E, Lawson W, Gilchrist M, Holmes AH. Effect of adding a mobile health intervention to a multimodal antimicrobial stewardship programme across three teaching hospitals: an interrupted time series study. J Antimicrob Chemother 2017;72(6):1825–31.https://doi.org/10.1093/jac/dkx040. [27] Herawati F, Yulia R, Hak E, Hartono AH, Michiels T, Woerdenbag HJ, et al. A
retrospec-tive surveillance of the antibiotics prophylactic use of surgical procedures in private hos-pitals in Indonesia. Hosp Pharm 2019;54(5):323–9. https://doi.org/10.1177/ 0018578718792804.
28. Yulia R, Giovanny BE, Khansa AA, Utami SP, Alkindi FF, Herawati F, Jaelani AK. The third-generation cephalosporin use in a regional general hospital in Indonesia. Int Res J Pharm 2018;9(9):41–5.https://doi.org/10.7897/2230-8407.099185.
29. Dellit TH, Owens RC, McGowan Jr JE, Gerding DN, Weinstein RA, Burke JP, Huskins WC, Paterson DL, Fishman NO, Carpenter CF, Brennan PJ, Billeter M, Hooton TM. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 2007;44(2):159–77.https://doi.org/10.1086/510393Epub 2006 Dec 13. 30. Eells SJ, Nguyen M, Jung J, Macias-Gil R, May L, Miller LG. Relationship between adher-ence to oral antibiotics and postdischarge clinical outcomes among patients hospitalized with Staphylococcus aureus skin infections. Antimicrob Agents Chemother 2016;60: 2941–8.https://doi.org/10.1128/AAC.02626-15.
31.Glanz K, Rimer BK, Viswanath K. Health behavior and health education: theory, research, and practice. . 4th ed.San Francisco, CA: Jossey-Bass; 2008.
32. Muñoz EB, Dorado MF, Guerrero JE, Martínez FM. The effect of an educational interven-tion to improve patient antibiotic adherence during dispensing in a community phar-macy. Aten Primaria 2014;46(7):367–75.https://doi.org/10.1016/j.aprim.2013.12.003 [Epub 2014 Feb 26].
F. Herawati et al. Health Policy OPEN 1 (2020) 100002
